An implicit and reliable neural measure quantifying impaired visual coding of facial expression: evidence from the 22q11.2 deletion syndrome

Abstract

Although various psychiatric disorders present with social-cognitive impairment, a measure assessing social-cognitive processes implicitly and reliably, with high selectivity and with enough signal-to-noise ratio (SNR) for individual evaluation of any population at any age, is lacking. Here we isolate a neural marker quantifying impaired visual coding of facial expression in individuals with 22q11.2 deletion syndrome (22q11DS) using frequency-tagging with electroencephalography (EEG). Twenty-two 22q11DS participants and 22 healthy controls were presented with changes of facial expression displayed at low, moderate, and high intensities every five cycles in a stream of one neutral face repeating 6 times per second (i.e., at a 6 Hz base rate). The brain response to expression changes tagged at the 1.2 Hz (i.e., 6 Hz/5) predefined frequency was isolated over occipito-temporal regions in both groups of participants for moderate- and high-intensity facial expressions. Neural sensitivity to facial expression was reduced by about 36% in 22q11DS, revealing impaired visual coding of emotional facial signals. The significance of the expression-change response was estimated for each single participant thanks to the high SNR of the approach. Further analyses revealed the high reliability of the response and its immunity from other neurocognitive skills. Interestingly, response magnitude was associated with the severity of positive symptoms, pointing to a potential endophenotype for psychosis risk. Overall, the present study reveals an objective, selective, reliable, and behavior-free signature of impaired visual coding of facial expression implicitly quantified from brain activity with high SNR. This novel tool opens avenues for clinical practice, providing a potential early biomarker for later psychosis onset and offering an alternative for individual assessment of social-cognitive functioning in even difficult-to-test participants.

Facial Expression Processing Across the Autism–Psychosis Spectra: A Review of Neural Findings and Associations With Adverse Childhood Events

“…Interestingly, this study revealed significantly reduced emotion discrimination responses in the patient group (in particular for anger, disgust, and sadness) while showing slightly increased general visual face processing responses. Moreover, the neural response magnitude to expression changes was inversely associated with the severity of positive symptoms, pointing to a potential endophenotype and/or biomarker for psychosis risk (147). In this regard, this study strongly points toward emotion-specific facial processing impairments in psychosisprone individuals while also echoing the findings of increased neural salience of faces per se.…”

“…A particularly promising approach for this would be the administration of a fast periodic visual stimulation oddball frequency-tagging paradigm, as has been applied in ASD (124,125). Thus far, this method has not been applied in primary psychosis, but it was recently administered in patients with velocardiofacial (22q11.2 deletion) syndrome, which is a well-known high-risk group for psychosis (147). Interestingly, this study revealed significantly reduced emotion discrimination responses in the patient group (in particular for anger, disgust, and sadness) while showing slightly increased general visual face processing responses.…”

“…However, it should be noted that the N170 is a very rough index that is not specific for facial expression processing and that lacks specificity, objectivity, sensitivity, and reliability, as pointed out in a number of recent reports (121,147,185,188). Most importantly, the N170 does not consistently categorize individuals and does not measure a specific impairment (facial expression processing) related to a specific clinical profile (e.g., ASD).…”

“…In the past years, an alternative EEG approach, called fast periodic visual stimulation frequency-tagging EEG, has been put forward, yielding promising findings pinpointing selective facial expression processing impairments in individuals with ASD (124,125) and primary psychosis (147). This novel approach reveals an objective, selective, reliable, and behaviorfree signature of impaired visual coding of facial expression, implicitly quantified from brain activity with high signal-to-noise ratio at the individual subject level.…”

Exploratory case study of monozygotic twins with 22q11.2DS provides further clues to circumscribe neurocognitive markers of psychotic symptoms

“…A fast periodic visual stimulation coupled with EEG was used to implicitly measure the detection of brief changes of facial expression (anger, disgust, fear, happiness and sadness) at different intensity levels (20%, 60%, 100%). This paradigm was adapted from previous studies (Leleu et al, 2018, Leleu et al, 2019), and details of the procedure and data acquisition are available in the supplementary file. Briefly, neutral faces were presented at a base rate of 6 Hz and expressive faces were introduced at a lower rate of 1.2 Hz (i.e., every 5 stimuli).…”